A<i>Caenorhabditis elegans</i>RNA-Directed RNA Polymerase in Sperm Development and Endogenous RNA Interference

Gent, Jonathan I.; Schvarzstein, Mara; Villeneuve, Anne M.; Gu, Sam Guoping; Jantsch, Verena; Fire, Andrew; Baudrimont, Antoine

doi:10.1534/genetics.109.109686

Cited by 87 publications

(111 citation statements)

References 78 publications

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“…Sperm genes are also overexpressed in eri-1 and rrf-3 mutants (Asikainen et al, 2007), both of which encode Dicer complex components that produce 26G endo-siRNAs complementing spermatogenesis genes (Gent et al, 2009;Han et al, 2009;Pavelec et al, 2009). It has been proposed that spermatogenesis defects observed when impairing ERI-1, RRF-3 or the sperm-specific 26G-binding proteins ALG-3 and ALG-4 can be attributed to either under-or overexpression of sperm mRNAs (Conine et al, 2010;Gent et al, 2009;Han et al, 2009;Pavelec et al, 2009). This apparent discrepancy might have a simple resolution if an endogenous siRNA pathway represses sperm-specific transcription in adult hermaphrodites that have already undergone spermatogenesis, but promotes sperm-specific transcription in males and during the short window of spermatogenesis in hermaphrodites.…”

Section: Discussionmentioning

confidence: 99%

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Campbell

Updike

2015

Development

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Germ granules (P granules) in C. elegans are required for fertility and function to maintain germ cell identity and pluripotency. Sterility in the absence of P granules is often accompanied by the misexpression of soma-specific proteins and the initiation of somatic differentiation in germ cells. To investigate whether this is caused by the accumulation of somatic transcripts, we performed mRNA-seq on dissected germlines with and without P granules. Strikingly, we found that somatic transcripts do not increase in the young adult germline when P granules are impaired. Instead, we found that impairing P granules causes sperm-specific mRNAs to become highly overexpressed. This includes the accumulation of major sperm protein (MSP) transcripts in germ cells, a phenotype that is suppressed by feminization of the germline. A core component of P granules, the endo-siRNA-binding Argonaute protein CSR-1, has recently been ascribed with the ability to license transcripts for germline expression. However, impairing CSR-1 has very little effect on the accumulation of its mRNA targets. Instead, we found that CSR-1 functions with P granules to prevent MSP and sperm-specific mRNAs from being transcribed in the hermaphrodite germline. These findings suggest that P granules protect germline integrity through two different mechanisms, by (1) preventing the inappropriate expression of somatic proteins at the level of translational regulation, and by (2) functioning with CSR-1 to limit the domain of sperm-specific expression at the level of transcription.

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Section: Discussionmentioning

confidence: 99%

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Campbell

Updike

2015

Development

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“…There are multiple endo-siRNA pathways in C. elegans, including the CSR-1 RNAi pathway (Claycomb et al 2009;Gu et al 2009), the WAGO RNAi pathway , and the ERI RNAi pathway Gent et al 2009;Han et al 2009;Vasale et al 2010). The biological roles of the endo-RNAi pathways in C. elegans remain largely uncharacterized.…”

Section: Discussionmentioning

confidence: 99%

“…A major known role of the WAGO endoRNAi pathway is in genome surveillance: the silencing of transposable elements, aberrant transcripts , and gene duplications (Vasale et al 2010;Fischer et al 2011). The ERI pathway has been implicated in regulating genes required for spermatogenesis and fertility (Gent et al 2009;Han et al 2009;Conine et al 2010), whereas the CSR-1 RNAi pathway has been recently shown to positively regulate histone mRNA expression (Avgousti et al 2012).…”

Section: Discussionmentioning

confidence: 99%

Neuronal Migration Is Regulated by Endogenous RNAi and Chromatin-Binding Factor ZFP-1/AF10 in Caenorhabditis elegans

Kennedy

Grishok

2014

Genetics

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Endogenous short RNAs and the conserved plant homeodomain (PHD) zinc-finger protein ZFP-1/AF10 regulate overlapping sets of genes in Caenorhabditis elegans, which suggests that they control common biological pathways. We have shown recently that the RNAi factor RDE-4 and ZFP-1 negatively modulate transcription of the insulin/PI3 signaling-dependent kinase PDK-1 to promote C. elegans fitness. Moreover, we have demonstrated that the insulin/IGF-1-PI3K-signaling pathway regulates the activity of the DAF-16/FOXO transcription factor in the hypodermis to nonautonomously promote the anterior migrations of the hermaphroditespecific neurons (HSNs) during embryogenesis of C. elegans. In this study, we implicate the PHD-containing isoform of ZFP-1 and endogenous RNAi in the regulation of HSN migration. ZFP-1 affects HSN migration in part through its negative effect on pdk-1 transcription and modulation of downstream DAF-16 activity. We also identify a novel role for ZFP-1 and RNAi pathway components, including RDE-4, in the regulation of HSN migration in parallel with DAF-16. Therefore, the coordinated activities of DAF-16, ZFP-1, and endogenous RNAi contribute to gene regulation during development to ensure proper neuronal positioning.

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“…Most of these small RNAs start with G and are either 22 nt or 26 nt in length, reminiscent of C. elegans 22G-and 26G-RNAs. C. elegans 22G-RNAs function in chromosome segregation, transposon silencing, and gene regulation (Ambros et al 2003b;Lim et al 2003;Ruby et al 2006;Pak and Fire 2007;Sijen et al 2007;Claycomb et al 2009;Gent et al 2009;Gu et al 2009;van Wolfswinkel et al 2009;Vasale et al 2010;Zhang et al 2011) C. elegans has two classes of 26G-RNAs that regulate gene expression associated with spermatogenesis (Class I) and early zygotic development (Class II) Conine et al 2010;Gent et al 2010;Vasale et al 2010;Zhang et al 2011).…”

Section: Ascaris Endo-sirnas In Gametogenesis and Embryogenesismentioning

confidence: 99%

Deep small RNA sequencing from the nematodeAscarisreveals conservation, functional diversification, and novel developmental profiles

Wang

Czech²,

Crunk³

et al. 2011

Genome Res.

161

189

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Eukaryotic cells express several classes of small RNAs that regulate gene expression and ensure genome maintenance. Endogenous siRNAs (endo-siRNAs) and Piwi-interacting RNAs (piRNAs) mainly control gene and transposon expression in the germline, while microRNAs (miRNAs) generally function in post-transcriptional gene silencing in both somatic and germline cells. To provide an evolutionary and developmental perspective on small RNA pathways in nematodes, we identified and characterized known and novel small RNA classes through gametogenesis and embryo development in the parasitic nematode Ascaris suum and compared them with known small RNAs of Caenorhabditis elegans. piRNAs, Piwi-clade Argonautes, and other proteins associated with the piRNA pathway have been lost in Ascaris. miRNAs are synthesized immediately after fertilization in utero, before pronuclear fusion, and before the first cleavage of the zygote. This is the earliest expression of small RNAs ever described at a developmental stage long thought to be transcriptionally quiescent. A comparison of the two classes of Ascaris endo-siRNAs, 22G-RNAs and 26G-RNAs, to those in C. elegans, suggests great diversification and plasticity in the use of small RNA pathways during spermatogenesis in different nematodes. Our data reveal conserved characteristics of nematode small RNAs as well as features unique to Ascaris that illustrate significant flexibility in the use of small RNAs pathways, some of which are likely an adaptation to Ascaris' life cycle and parasitism.

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ACaenorhabditis elegansRNA-Directed RNA Polymerase in Sperm Development and Endogenous RNA Interference

Cited by 87 publications

References 78 publications

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Neuronal Migration Is Regulated by Endogenous RNAi and Chromatin-Binding Factor ZFP-1/AF10 in Caenorhabditis elegans

Deep small RNA sequencing from the nematodeAscarisreveals conservation, functional diversification, and novel developmental profiles

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